Journal of Mathematical Sciences, Vol. 93, No. 4, 1999
THE ROLE OF SEX CHROMOSOMES IN EVOLUTION: A NEW CONCEPT
V. A. Geodakian (Moscow, Russia)
UDC 57.011+576.316.74
Sex differentiation allows us to check evolution innovations in the male genome before their
transmission to the female one. This is possible under asynchronous evolution, since the male
evolution precedes the female one. The asynchronicity means that there should be exclusively male
genes, which present in the male genome but are absent from the female genome yet, and exclusively
female genes, which the male genome has lost but which still exist in the female genome; this is also
referred to as the genotypic sexual dimorphism. Treating the dimorphism as a consequence of the
sexual dichronism, we are able to reveal the evolution roles of the sex chromosomes and suggest a
new concept, which asserts that the Y-chromosome plays the role of a “gate” to feed the input
information into, the role of the place where new genes are formed and verified, and the role of
initiator, accelerator, and regulator of genotypic sexual dimorphism. On the other hand, the Xchromosome is treated as a “transport” which translocates new genes from the Y-chromosome to the
autosomes, stabilizes and smoothens the sexual dimorphism, and stores old genes which have to be
eliminated. The suggested concept gives a new understanding of the genesis, localization, and
transferring of genes, as well as of the phenomena of chromosome inactivation, mobile genes,
relation of the Y-chromosome to stresses, retroviruses, etc.
1.
Introduction
Since the discovery of the sex chromosomes due to McClung [7], it has been assumed that their primary role
consists of the sex determination and the maintenance of a 1 : 1 sex ratio. But is this actually so? Sex
chromosomes do perform both of these functions, but this does not necessarily mean that such is their
principal functional significance. Indeed, a single autosomal trigger gene is quite enough to control sex
determination, and the sex ratio of 1 : 1 naturally arises from the progeny from crossing between a recessive
homozygote and a heterozygote. In this context, it is unclear what the evolutionary purpose of differentiation
into autosomes and sex chromosomes is. On what principle is it based? What particular genes are located
on autosomes and on the X and Y chromosomes? How can we explain the features of sex chromosome
pairing, crossing-over, translocation, and condensation? What are the results of different algorithms of
chromosome behavior? Why are the autosomes transferred from the parents to the descendants in a
stochastic manner, whereas the sex chromosomes behave in special ways, namely, the Y-chromosome is
transferred from the father to the son only and the X-chromosome, to the daughter? Which genes are
localized in autosomes, X-chromosomes, and Y-chromosomes, respectively? We know much about how the
genes work in ontogenesis, but know almost nothing about their “living” in the genome in phylogenesis:
whether they lead a settled life (are born, live, work, and die in a single chromosome) or nomadize? Is there
a regular route of the genes via the chromosomes, and if yes, what is such a route?
Data accumulated to date present many problems and discrepancies which cannot be explained in the
context of the existing theory of sex chromosomes. For example, inactivation of one X-chromosome in
somatic cells of females, manifested in the presence of the Barr bodies (condensed, inactive sex chromatin),
has been interpreted as a mechanism for compensating for the dosage for X-linked genes. If this were the
case, the Barr bodies would have been specific only for the homogametic sex. In birds, however, the
females have only one X-chromosome, but it becomes condensed as in mammals. This is by no means
dosage compensation. For some reason, sex chromosome pairing in birds is absent [8]. Again, for some
reason, replication of the DNA of a single X-chromosome in a homogametic sex and of the Y-chromosome
occurs only after autosome replication [8), etc.
The Y-chromosome is a very mysterious structure. This is the most variable chromosome of the genome
(particularly with respect to its length). It is rich in nucleotide repeats and heterochromatin (animals) and in
euchromatin (plants). In plants, similar repeats are distributed along all chromosomes of the genome [9].
The human Y-chromosome is almost empty (except for the ear hairiness or the web genes), but in other
species it can contain a number of active genes. For example, Drosophila possesses many genes linked to the
Y-heterochromatin. In guppies, more than 30 Y-linked genes (and only one autosome-linked gene) that
determine the body color of males have been identified. Some of these genes are involved in unequal
crossing-over with the X-chromosome (Y→X recombination is four times more frequent than it’s X→Y
counterpart) [10, 11]. Studies of dragonflies led to the conclusion that, in the evolutionary sense, the XY
system of sex chromosomes is younger than the XO system. Nevertheless, according to another concept, sex
chromosomes originated from a pair of autosomes carrying sex-determining genes. That is why the Ychromosome of certain (usually more primitive) species is similar in size to the X-chromosome, conjugates
with the latter completely or partially, and participates in crossing-over. As concerns other, more advanced
species, the Y-chromosome is small and pairs with the X-chromosome end to end, without crossing-over.
For some reason, evolution was accompanied by the loss of active genes from the Y-chromosome, leading to
its degradation and eventual disappearance. The XY system is hence regarded as a system that precedes the
XO one [12]. This concept seems to be favorable; we disagree with it in only one point. It was suggested
there that a bright red spot, currently specific for male guppies, was initially present in fish of both sexes,
but females lost it during evolution. From our viewpoint, females never had such a spot. Other data on the
Y-chromosome concern its larger size in different ethnic or social groups, its high variability in rodents that
inhabit zones of increased seismic activity [13], its association with retroviruses [14], and its connection
with new mutations [15, 16].
It seems likely that our knowledge of sex chromosomes, primarily of the Y-chromosome, lacks something
essential. The main point is what are these chromosomes for? What are their functional roles, adaptive
value, and evolutionary significance? What logic is in their existence?
In this paper, we propose a new concept concerning sex chromosomes, namely an information model based
on the idea of their asynchronous evolution.
2.
What is the Sex for?
First, we have to answer the fundamental question: what is the sex for?
During the last century, the sex problem remained a central problem of the theory of evolution. The
foremost specialists of the nineteenth and twentieth centuries, Darwin, Walles, Weismann, and Fisher, dealt
with this problem. Nevertheless, today scientists still speak about the crisis in evolution theory related to the
sex. In the last two decades, the sex problem has been revived again. Dozens of books have appeared
concerning this problem [17-26]. Let us cite several of them: “The dominance of sexual, reproduction in
plants and animals is not consistent with the modern evolution theory”; "We have no satisfactory
understanding why the sex appeared and survived”; "The sex is the main challenge in the modern evolution
theory; Darwin's and Mendel's insights, which solved so many puzzles, have no success in the secret of
sexual reproduction.”
Many papers and surveys are related to this problem. At least two leading genetic journals devoted special
issues to the sex problem [27, 28]. This indicates that the central problem of evolution theory and genetics
is still unsolved in the Western world [29]. No one knows yet what the sex is for!
The author felt these basic deficiencies in the beginning of the sixties; the first, somewhat heuristic, version
of the solution of this problem was suggested in 1965 in [1].
The most fundamental objective of life is the reproduction program, which lies at the heart of such
phenomena as replication, reduplication, and asexual reproduction. This is the basic criterion to distinguish
the living systems from the others. The main source of variations under this program consists of mutations.
The subordinate objective consists of a recombination program that underlies such phenomena as crossing-
over, fertilization, or syngamy. By creating a new source of variations, not depending on the environment,
the problem of realizing diversification was completely solved. On this basis, the sexual process arose. The
third most important objective consists of the differentiation constituting the heart of the meiosis
phenomenon, sexual differentiation, etc. As the result of this process, dioecious forms appeared, as well as
castes in social insects, dwarf males in some fish species, etc. In the evolution process, these programs, as
well as the biologic phenomena based on them, came into light in exactly this order, which reflects their
interrelations: the first are necessary for the succeeding to exist, but the presence of secondary ones is
facultative with respect to the preceding.
The sex notion consists of two fundamental phenomena: the sexual process (conjugation of genetic
information of two persons) and the sexual dimorphism (partitioning this information into two parts).
Depending on the presence (+) or absence (-) of these phenomena, the whole variety of existing reproduction
models can be divided into three basic forms: asexual reproduction (-, -), hermaphrodite reproduction (+, -),
and bi-sexual reproduction (+, +).
The sexual process and sexual differentiation are distinct, and moreover, directly opposite phenomena.
Indeed, the sexual process diversifies genotypes, which is its objective in evolution, whereas differentiation
halves the resulting diversity. So, in an asexual population of N persons the maximal quantity of genotypes
of the descendants is N, provided that the genotypes of the parents are distinct. Because the progeny of each
asexual person is a clone of the same genotype, the diversity σ, of the progeny cannot exceed N. Under the
bi-sexual process, the diversity of the progeny is the squared cardinality of the set of parents' genotypes. As
concerns hermaphrodites, each person can couple with N - 1 persons (except itself); we hence conclude that
σ = N(N - 1)/2 ≈ N 2/2 as N >> 1. Under bi-sexual reproduction, where the combinations of two persons of
the same sex are not allowed, the diversity is at least halved: σ = (N/2) * (N/2) = N 2/4 (each female couples
with each male, and there are N/2 persons of each sex). The diversity of the progeny depends on the sex
ratio of the parent generation, and attains its maximum at the 1 : 1 sex ratio.
Thus, for the strength N of the parent generation fixed, the maximum progeny diversity of the asexual,
hermaphrodite, and bi-sexual populations are related as N : N 2/2 : N 2/4, i.e., the diversity is at least halved
while passing from hermaphrodite to bisexual reproduction! Then, it becomes completely unclear what the
differentiation is intended for, if it halves the main bonus provided by the sexual process. Why are all
progressive species bi-sexual, since the asexual process is much more efficient and simple, and
hermaphrodites possess a more diversified progeny? This is the essence of the sex puzzle. The fact that this
problem is still unsolved is primarily due to the lack of a clear understanding that the sexual process and
sexual differentiation are opposite phenomena. Researchers make attempts at understanding the advantage
of the sexual reproduction (hermaphrodite and bi-sexual forms) over the asexual one, although it is
necessary to understand the advantage of bi-sexuals over hermaphrodites. The purpose of the sexual process
is clear, and consists of diversifying. It is needed to comprehend the objective of the sexual differentiation.
Although it is recognized that, because bi-sexual methods have no visible advantages over asexual ones, bisexual reproduction should provide us with significant evolutionary bonuses, the sex problem is commonly
considered as a reproduction problem but not an evolutionary one.
3.
Idea of Asynchronous Evolution
In the framework of Darwinian adaptogenesis, evolution of a system ensues from changes in the
environment and progresses by way of trial and error. It is hence more advantageous to "experiment” with
only a part of the system, rather than with the whole aggregation. To do this, the system should be
subdivided into two subsystems. The first should be "removed” (protected) from the environment to
preserve the past, and the second should be widely exposed to the environment to know better what is
required at present and may prove necessary in the future. Such a conservative-operative specialization of
parts (sexes) is achieved by their asynchronous evolution [1]: the new features first manifest themselves in
the operative subsystem (the male part) and are then tested and passed to the conservative subsystem (female
part).
In 1972, the author generalized this idea, applying it to a conservative-operative interpretation of various
evolving binary adaptive systems, from molecular to population and social: DNA-proteins, autosomes-sex
chromosomes, nucleus-cytoplasm, gametes-somatic cells, female-male sex, brain cortex-subcortex, etc. In
addition, a hypothesis was formulated that all differentiations can be considered as operative-conservative
specializations which determine the method of information distribution over subsystems [30]. On this basis,
isomorphic theories were suggested that concern asynchronous evolution of sexes [2-5], and the asymmetry
of organism, brain, and handedness [31]. These theories were regarded as having an exceedingly high (for
biological theories) explanatory and prognostic potential [32]. Further, an attempt was made to extend this
approach to the autosome-sex chromosome differentiation [6].
The essence of the theory proposed can be formulated as follows. A bisexual population becomes
subdivided into females and males; a bilateral organism, into left and right halves; the brain, into the left and
right hemispheres, the genome, into autosomes and sex chromosomes; and sex chromosomes, into the Xand Y-chromosomes, etc. All these differentiation processes are based on the same specialization principle
of conservation and variation, which both necessarily underlie the evolution process. If one of the two bases
vanishes, the evolution stops, because the system either degenerates or becomes stable. Their ratio
characterizes the evolutionary flexibility of the system. They are complementary: the more the conservation,
the smaller the variation, and vice versa. Without subsystem specialization, the system should maintain
some optimal ratio between conservation and variation, whereas both of them can simultaneously be made
greater in the case where the subsystems become specialized. So the advantage of differentiation manifests
itself.
In each of the above-mentioned systems, the first system is conservative, basic, protected from the
environmental influence, whereas the second is operative, experimental, widely open to environmental
factors. The information from the environment is first fed into the operative subsystem, which then
transmits it to the conservative one. They hence evolve asynchronously: the former commence and
complete their evolution earlier than the latter.
Hence, new traits first appear in males and become transmitted to females only after many generations [2,
3]; new functions initially develop on the right-hand side of the body and later, on the left-hand side;
dominant nerve centers controlling these functions appear in the left hemisphere of the brain and only then
become transferred to the right one [31]. Likewise, new genes first appear in the Y-chromosome and then,
after many generations, become transmitted through the X-chromosome to autosomes [6].
The theory of asynchronous evolution of sexes regards differentiation between them as a rather economical
type of information contact of a population with the environment. Male and female sexes respond to the
effect of ecological differential (directional selection) in different ways. In 1974, the author formulated a
hypothesis on a wider reaction norm of females as compared to males, which allowed one to predict the
greater concordance of male pairs of monozygote twins and dizygote female pairs [33]. A wider reaction
norm of females allows them to develop an adaptive phenotype on the basis of their existing genotype due to
the ontogenetic flexibility only, and to escape from selection pressure. Males, with their narrow reaction
norm, have no such possibility. As a result, the ecological differential affects largely males. Their number
decreases, and the distribution of genotypes changes, i.e., one and the same ecological information modifies
females and eliminates males. In other words, the sexual dimorphism provides females with phenotypic
plasticity in ontogenesis, and males, with genotypic plasticity in phylogenesis, resulting in their faster,
"look-ahead" evolution. Females hence convert ecological information into temporary phenotypic sex
dimorphism. Males, at the expense of their abundance, convert this information into genotypic sexual
dimorphism, thereby testing and then safely transmitting it to females. In this way, the genotypic sexual
dimorphism, rather than the ecological differential, becomes the intrapopulation driving force for females,
allowing them to receive ecological information from the male sex without any selection pressure. This is
exactly the evolutionary sense of the sexual differentiation and the main advantage of bi-sexual forms.
According to our theory, the evolution of any trait can be divided into three stages.
At the initial, divergent stage, the trait changes in males only. The genotypic sexual dimorphism appears
and improves in a series of generations. The duration of the divergent phase (asynchronism, or sexual
dichronism) is equal to the lag in the evolution of female genotype. This period is necessary to test new
genes within the male genotype. But sex divergence cannot develop ad infinitum; otherwise sexes would
become reproductively isolated. Consequently, the mechanism of dimorphing relaxation is switched on,
which consists of the information flow from the male sex to the female one. From then on, evolution of the
trait in females begin. This is the parallel stage, when the trait evolves in both sexes at the same rate, and
the genotypic sexual dimorphism process remains in the stationary state. The third, convergent stage of
evolution begins when males are no longer affected by the ecological differential, whereas females are still
under the effect of genotypic sexual dimorphing. The genotypic sexual dimorphism decreases and then
vanishes, the dimorphic trait becomes monomorphic (stable), and the evolution of the trait is thus complete.
The abovesaid means that the sexual dimorphism, which is commonly regarded as an effective way of
reproduction, is rather an effective way of evolution [2, 3]. It is natural that the new treatment of the basic
notion of sex allows us to consider from the new viewpoint the derivative notions of sex differentiation, sex
chromosomes, sex hormones, etc., which immediately take evolutionary meanings as well.
4.
Sexual Dimorphism
The only known explanation for the appearance of sexual dimorphism is given by the Darwinian sexual
selection theory [34]. But, explaining the general phenomenon of sexual difference as a consequence of a
particular mechanism of sex selection, Darwin made a methodological mistake, because a theory should be
wider than a phenomenon but not vice versa. But the sex selection theory cannot explain the existence of
sexual dimorphism in plants, which the sex selection is not applicable to, and can predict nothing about
traits that are not related to sex selection [35, 36].
According to the theory of asynchronous evolution of sexes, the sex dimorphism is a consequence of
asynchronous evolution of sexes, and hence it occurs only in evolving traits. It always takes place, during
evolution of any traits, as the "distance" between sexes under any selection, natural, sexual, artificial, etc.
The direction of sexual dimorphism, from the female form of a trait to the male one, shows the direction of
evolution of the trait.
If the new information Inew has been assimilated by males but is still absent from females, or if the old
information Iold is eliminated in males but still presents in females, then. this phenomenon is exactly the
genotypic sexual dimorphism. Therefore, the information contained in the male genome is Imale = Icommon +
Inew , whereas the information in the female genome is Ifemale = Icommon + Iold , where Icommon is the information
common for both sexes. During mixing of two populations (species, races, ethnoses) the common
information is mixed in the first generation of descendants, whereas the old and new information is
separated during the sexual dichronism over many generations.
This concept provides a natural and simple explanation of the differences, of inter-specific, inter-racial, or
international reciprocal hybrids which are related to the hybridization direction, because the reciprocal
hybrids possess the common Icommon , and get Inew and Iold from different forms (compare the hinny and mule).
If the descendants obtained identical information from the father and mother, then there should be no
reciprocal phenomena.
The theory of asynchronous sex evolution provides, first of all, a natural and adequate explanation (based on
the unified standpoint) for a vast variety of poorly understood and mysterious phenomena and findings. For
example, the evolution of most vertebrates is accompanied by enlargement of sons, whereas most insects
and arachnids become smaller. Therefore, vertebrate males should be larger than females, whereas male
insects and arachnids should be smaller than females. It is exactly so. Also, we easily understand the
known superiority of male specimens (in all breeding parameters) described for all cultural animals, and are
able to predict the reciprocal paternal effect (dominance of male genotype) for all new traits (including
purely female traits). Indeed, the paternal effect is described with respect to egg-laying and milking
qualities. This theory adequately explains a number of mysterious phenomena in anthropology, with regard
to migration (both sexes of an ethnos are involved), conquest (conquerors are males, whereas the enslaved
ethnos consists of two sexes), and migration of slave women to the conquerors' land (two female and one
male ethnoses), etc. For example, Pavlovskii used the method of generalized portrait to study a Turkmen
population and found that portraits of women readily fit into a single type, whereas those of men belong to
two types [38]. In craniological studies on Bashkirs, Yusupov observed a unimodal distribution of
craniological parameters in women and a tetramodal distribution in men [39]. Dolinova and Kavgazova
performed studies in Udmurt and Bulgarian populations, respectively, and discovered sexual dimorphism in
dermatoglyphic patterns: male and female patterns had features characteristic of different adjacent ethnic
groups [40].
5.
Autosome-Sex Chromosome Differentiation of Genome and Evolution Phases
The author used the idea of asynchronous evolution for the first time in 1965, when interpreting the problem
of sex. At the same time, the author understood that this phenomenon underlies the differentiation into
autosomes and sex chromosomes, and concluded that in the chromosome set, the role of sex chromosomes
and autosomes is, in effect, respectively, the short-term and long-term memory; that is why sex
chromosomes, primarily the Y-chromosome, serve as a gateway into heredity for variation [1]. The results of
recent studies on the base substitution rate [15, 16] perfectly confirm this theoretical prediction.
When a system is partitioned into subsystems, the first question that arises in this connection concerns the
order of feeding the control environmental information into these subsystems. The information is always
fed first into the operative subsystem, and then is transmitted to the conservative part [30]. As concerns the
scheme of sexual dimorphism, the information goes as follows: environment → male sex → female sex. If
we consider the dimorphism of the brain, the information path is environment → left hemisphere → right
hemisphere. If the chromosome differentiation is similar to the sexual one, then this isomorphism can be
used to reveal the evolutionary role of autosomes and sex chromosomes on the basis of the approach
proposed above. To this end, we compare the male and female sexes, sex chromosomes and autosomes with
respect to their “informational behavior" (algorithm), i.e., their roles in receiving information from the
environment, processing it into pheno- or genotypic information, and transmitting to the progeny.
In the informational behavior of chromosomes, we can distinguish vertical and horizontal algorithms. The
former refer to the transmission of chromosomes in a series of generations, and the latter concern the
information exchange between chromosomes and environment via mutagenesis, crossing-over, translocation,
transfer by viruses, mobile genes, etc. There are three possible types of vertical transmission of chromosome
information:
stochastic algorithm from father and mother to descendant with equal probability;
ipsi algorithm to the descendants of the same sex;
contra algorithm to the descendants of the opposite sex.
The stochastic algorithm transfers the autosomes and X-chromosome of the homogametic sex; the ipsi
algorithm is the Y-chromosome algorithm; the contra algorithm deals with X-chromosomes of the
heterogametic sex.
The stochastic algorithm deals with the genetic information that is common for both sexes, and implies gene
mixing during each fertilization, which maximizes the monomodal genetic diversity, homogenizes the
population, and hence cannot provide a basis for genotypic sexual dimorphism. This algorithm is the most
aged, existing even before differentiation, and realizes only the reproduction and recombination programs.
Nonstochastic algorithms came into light after the appearance of different sexes, and deal with the
information which differs in mates and females, i.e., with genotypic sexual dimorphism; they hence produce,
maintain, and regulate the dimorphism.
Ipsi algorithms, pertaining to a single sex, transmit the genetic information via males, and hence can produce
genotypic sexual dimorphism and make it higher or lower. Ipsi algorithms initiate the differentiation
program.
Contra algorithms, like the stochastic ones, involve information transmission from one sex to another, hence
homogenizing the population, but, contrastingly, they maintain the genotypic sexual dimorphism at a stable
level rather than reduce it to zero.
The combination of ipsi and contra algorithms thus allows us to produce and maintain a certain difference
between subsystems, and vary it in dependence on the environmental condition. In this connection, contra
algorithms operate as stabilizers (negative feedback), while ipsi algorithms operate as regulators (positive
feedback) [41]. This maintains the evolutionary “distance" between the sexes.
This scheme also underlies the mystic but fundamental phenomenon that each of the hemispheres of the
brain controls the opposite half of the body. This scheme should also be in the heart of the mechanism that
regulates the sex hormones in males and females.
Let us sum up the sequence of actions of the algorithms to maintain asynchronous evolution.
1. In the divergence phase, in order for only the male evolution to take place and the genotypic sexual
dimorphism to be produced and enlarged, the new information from the environment should be
applied to the Y-chromosome only. It is clear that the objective of the divergence phase - the
transportation of the new information to the male genome, its accumulation there in the form of
genotypic sexual dimorphism, and verification - can be realized by Y-algorithm.
2. In the parallel phase, for the evolution of both sexes while the dimorphism remains constant, the new
information has to be transferred from the Y-chromosome to the female genome; this can be realized
by means of the contra X chromosome.
3. In the convergence phase, in order that only the female evolution should take place, while the
dimorphism vanishes, it is necessary to stop feeding the new information from the environment to the
Y-chromosome, but its transferring to the female genome via the contra X chromosome has to remain
active.
Any new gene, once occurring in the Y-chromosome, spends there a period equal to the dichronism duration
(many generations); only after the end of this period can it move away off the chromosome. This time is
necessary to verify the gene in the male genome. Under partial conjugation of the X- and Y-chromosomes
in both mammals and plants (e.g., guppies, melandrium), only a part of the genes are placed in the
conjugating section [9-11]. If the new genes went directly to this section, they could immediately be
included in the female genome, which is unallowable. Therefore, the input and output of the Y-chromosome
should be separated. The time which is necessary for a gene to move along the Y-chromosome in order to
attain the section which conjugates with the contra X chromosome is exactly equal to the duration of the
dichronism. Therefore, only those genes which have been verified in the Y-chromosome become transferred,
via unequal crossing-over between the Y- and X-chromosomes, into the female genome. It seems likely that
the input and output of the contra X chromosome are separated from one another, and, moving along the Xchromosome, the “newborn" gene is again verified in the male genome (in the homozygote state).
Therefore, before appearing in the autosomes, each new gene is tested twice in sex chromosomes - first in
the Y- and then in the X-chromosome. As concerns the recessive X-genes, they manifest themselves almost
exclusively in males, and only males are under selection pressure.
Thus, the gene pool of a sexually dimorphic population includes the following three groups of genes, which
differ in their evolutionary age and location.
1. The exclusively male Y- and X-genes (new, young genes “of tomorrow") are those that appeared in
males but have not yet been under selection and come to the female genome on their way to
autosomes.
2. The common genes (active, working genes “of today") are those making up the bulk of structural
autosomal genes equally represented in both sexes.
3. Exclusively female X-genes (old, used-up genes “of yesterday") are those already lost from the male
genome but still retained by the female genome as atavistic features. The necessity of these genes
follows from the theory and some well-known facts of anthropology. It seems likely that these genes
are localized in a special section of the X-chromosome (or in autosomes), and they move to the male
genome only to be then eliminated.
We note that under mixing of populations, the common genes are mixed in the first generation, while the
male and female ones, being transferred by the ipsi algorithm, remain separate during the genotypic sexual
dimorphism. As we have said, if the environment varies, then the females escape from selection pressure,
whereas males have no such possibility due to their narrower reaction norm. Therefore, the genotypic sexual
dimorphism in the reaction norm should exist in advance (in a stable phase). In addition, the genetic
information on a wide reaction norm should be transmitted via the female line, and the information on the
narrower norm, via the male line. This can again be done only by means of ipsi algorithms.
But why do the males possess a narrow reaction norm and operative specialization? Is there an opposite
situation?
Let us consider the reversion of sexual dimorphism under polyandry.
Polyandry, under which the female is coupled with several males, and hence a female possesses a higher
reproductive index than a male, is described in invertebrates, fish, birds, and mammals. Then, a reversion of
sexual dimorphism frequently occurs: females are larger than males and have a brighter coloring, males
build the nest and care for the descendants, etc. Under polygyny, the picture is reversed. This means that the
direction of sexual dimorphism, and hence of asynchrony, and the ratio of evolution rates of the sexes
depend on the polygamy direction, or the ratio of reproductive indices of the sexes. In a strictly
monogamous population, males and females possess identical indices, i.e., there are as many fathers as
mothers; then the variances of ipsi chromosomes of sons and daughters are equal as well. Under polygyny,
when there are fewer fathers than mothers, the variance of sons' Y-chromosomes is less than that of
daughters' ipsi X chromosomes. Under polyandry, the situation is reversed. Therefore, the variance of sons'
Y-chromosomes is proportional to the number of fathers, whereas that of daughters' ipsi X chromosomes is
proportional to the number of mothers.
On the other hand, as we have seen above, to ensure that the sexual dimorphism precedes the evolution of
any trait, it is necessary to satisfy the following conditions:
1. The reaction norm is inherited by means of the ipsi algorithm (Y- and X-chromosomes).
2. The reaction norm width is regulated by the sex hormones, because, according to the theory of
asynchronous sex evolution, the sex hormones are those agents which regulate the “distance" between
the system and environment: androgens bring the system “nearer" to the environment, and estrogens
do the reverse operation. Moreover, it is known that the Y-chromosome initiates the synthesis of
testosterone, being the agent whose concentration determines the sexual dimorphism.
This allows us to suggest the hypothesis that the reaction norm is determined by the sex hormones, and its
width is inversely related to the testosterone concentration. We can hence relate the direction of genotypic
sexual dimorphism, i.e., the ratio of evolution rates of males and females, to the ratio of their reproductive
indices.
Therefore, the part of the evolution vanguard is always played by a more heterogamous sex, and that of the
rear guard, by a monogamous one. The reason why polygyny is more widespread whereas polyandry
remains exotic is because of the higher reproductive potential of males. Rigorously speaking, there is no
polyandry but oligoandry, because the potentialities of females are limited.
Thus, the vitality, which is closely related to the reaction norm, is higher in females in the progeny of a
single father and many mothers, and in males in the progeny of a single mother and many fathers.
Let us give a general picture of how a single gene moves along the genome pool chromosomes. We enclose
hypothetical elements in brackets. If a new gene appears, we see the following: environment → cytoplasm
→ Y-chromosome → contra X male chromosome → contra X female chromosome → (ipsi X chromosome)
→ autosomes. The process of elimination of a “yesterday" gene looks as follows: autosomes → ipsi X
chromosome → contra X female chromosome → contra X male chromosome. Therefore, since sex
differentiation is accompanied by dichronomorphism of traits, chromosome differentiation should be
likewise accompanied by oligochronomorphism of genes, i.e., one and the same gene should appear at threefour different moments and in the same number of forms (namely Y, contra X, autosome, ipsi X).
Moreover, vectors of the evolution of chromosomal oligomorphism (ipsi X → A → contra X → Y), as in the
case of sexual dimorphism (female → male), are always opposite to the information flow (Y → contra X →
A → ipsi X; male → female), and can serve as a compass of evolution.
Autosomes provide long-term memory in the sexually dimorphic genome (as the female sex does in a
population), store the working structural genes common for both sexes, and thereby serve for genome
conservation. From the phylogenetic viewpoint, they are the oldest chromosomes, found even in sexless
organisms. Autosomes contain fundamental species-specific information, and implement the reproduction
and recombination programs, which are somewhat ancient. Stochastic transmission of autosomes ensures the
maximum diversity of genotypes. Owing to that, autosomes perfectly fulfill the programs of the sexual
process (fertilization), in which remarkable achievements are made by hermaphrodites. In this sense,
autosomes can be regarded as recombination chromosomes.
Sex chromosomes are short-term memory structures, the experimental subsystem of the genome (a male sex
analogue), and provide for genome modification. Their main role is to make evolution more efficient. From
the phylogenetic viewpoint, sex chromosomes appeared together with sexual dimorphism, which means that
they are significantly younger than autosomes. By triggering and implementing the differentiation program,
sex chromosomes form two subsystems in a population, based on the conservation-variation principle, and,
depending on the extent of polygyny-polyandry, i.e., on the “diameter of the pipe" to transmit genetic
information to the progeny, distribute the corresponding roles among the subsystems. To this end, more
monogamous and more heterogamous sexes acquire a wide and narrow reaction norm, respectively,
independently of their homo- or heterogamety [33]. This results in the formation of two independent,
asynchronously evolving systems separated by an information barrier. By regulating the rate of information
transmission, sex chromosomes control the amount of information fed into the genome. They contain mainly
evolving genes, both newly acquired and bound to be lost. Sex chromosome functioning contravenes the
recombination program, forbidding male-male and female-female combinations, and reduces the genotypic
diversity resulting from the sexual process. In this sense, they are more “antisex” than “sex” chromosomes.
It is more logical to call them the evolutionary chromosomes, according to their role.
The Y-chromosome is a link between the nucleus and cell environment (cytoplasm, mitochondria, etc.), a
kind of genomic gateway for information. Incidentally, the incompatibility of the Y-chromosome of one
Drosophila line with the cytoplasm of another line is a criterion of reproductive incompatibility between the
lines [40]. This chromosome converts ecological information into a genomic format, i.e., it produces new
genes (mutations) and can hence be named the ecological chromosome. It initiates the synthesis of male
hormones and thus determine the male reaction norm; contains “tomorrow" genes; triggers, accelerates, and
controls the development of asynchronism or sexual dichronomorphism; and serves as a primary “test
laboratory" and “quarantine" for new genes.
The contra X chromosome is a gene carrier linking the Y-chromosome with the female genome (i.e., the
transport chromosome). From the phylogenetic viewpoint, it functions as a stabilizer, relaxer, and liquidator
of sexual dichronomorphism. It also tests new genes (hemizygous in males) once more during ontogenesis.
It is likely that there the old genes moved from autosomes are eliminated, because this way is open to intense
selection.
The ipsi X chromosome (more exactly, a certain region of it) is involved in determining the reaction norm in
females, depending on the type of polygamy, and also determines the sex hormones. The X-chromosomes
contain a relatively high proportion of modification genes of quantitative traits.
Let us speculate which genes lie in autosomes and sex chromosomes. The existing theory of sex
chromosomes gives us no clear answer. The names of the chromosomes imply that the autosomes contain
somatic genes that do not depend on sex, and the sex chromosomes contain the generative genes that relate
to sex and reproduction. The theory suggested here immediately gives us the following clear answer: the
autosomes contain philogenetically old genes, and the sex chromosomes, new ones. Thus, the genetic pool
can be divided into four groups:
1. Somatic old genes.
2. Generative new genes.
3. Generative old genes.
4. Somatic new genes.
Only last two groups are informative, the two theories applied to them give diametrically opposite
implications. The existing theory asserts that the generative old genes are in the sex chromosomes and the
somatic new genes are in the autosomes, whereas the theory proposed here states the contrary, that the
generative old genes are placed in the autosomes, and the somatic new genes are in the sex chromosomes. It
is clear that all thirty genes of guppies' coloring (except for one autosome), as well as the Y-genes of webs or
ear hairiness in humans, should be regarded as somatic new ones, because the former are the result of
artificial selection of new traits which are absent from wild guppies, and the latter are new somatic
mutations. Both of them are phylogenetically young and have no relation to the reproductive function. These
facts corroborate the new theory proposed by the author.
Experimental results confirming the idea of asynchronous evolution of sexes, proposed in 1965, were first
obtained in 1987 [15]. It is known that the number of cell divisions during spermatogenesis is much greater
than during oogenesis, and errors in DNA replication and repair are the main source of mutations in
molecular evolution. On this basis, it was suggested that the mutation frequency in sex chromosomes is
greater than in autosomes and that, at least in the evolution of mammals, males serve as mutation generators
(note that a higher level of spontaneous and induced mutagenesis in both homo- and heterogametic males, as
compared with females, has been repeatedly demonstrated for Drosophila, silkworm, and mammals,
including humans [41]). By comparative analysis of nucleotide substitutions in human and mouse genes
located on autosomes and sex chromosomes, it was demonstrated that males do provide the main source of
mutations for molecular evolution, and that the ratio of gene evolution rates is Y : A : X = 2.2 : 1 : 0.6,
which conforms to the theoretical expectation 2 : 1 : 2/3 [15].
In another study, the same methods were used to compare Y/X ratios of nucleotide substitution rates in
synonymous genes of human, orangutan, baboon, and squirrel monkey. The results showed that the Y genes
diverge at a greater rate and farther from one another than the X genes [16]. Hence, molecular evolution
begins with males.
6.
Conclusion
The proposed concept allows an alternative interpretation of many obscure phenomena, including those
mentioned in the beginning of the paper. For example, X-chromosome condensation into the Barr bodies in
the female genome should be interpreted as a barrier to new information rather than gene dosage
compensation. The euchromatin nature of the Y-chromosome in plants and nucleotide repetitions distributed
over all chromosomes are due to the relatively new character of sexual differentiation in plants as compared
to mammals [7].
Being an ecological chromosome, the Y-chromosome should have a close relation to stress. A relationship
of that kind can explain such facts as the relatively larger size of the Y-chromosome in people of certain
ethnic (Jews) or social (prisoners) groups, or its higher variance in rodents that inhabit zones of increased
seismic activity; the higher variance of the Y-chromosome of those rodents is caused not by exposure to a
higher radiation of radon concentrations but by the simple stress due to frequent earthquakes. In this context,
we can predict the following:
 changes in the size or variance of the Y-chromosome in inhabitants of regions suffering from frequent
and powerful earthquakes, genocide, long wars, migrations, famine, and other natural or social
disasters;
 great ontogenetic (age-related) variation of the Y-chromosome;
 variability of the Y-chromosome in animals and plants that intensely evolve under artificial selection.
The close relation between the Y-chromosome and retroviruses demonstrated in [14] becomes more
comprehensive. (These authors isolated DNA from X- and Y-chromosomes of ten murine lines differing in
many traits, and then hybridized these samples with retroviral DNA. The results showed that, in all these
lines, the retroviral sequences are present in the Y-chromosome DNA but absent from the X-chromosome
DNA.)
In conclusion, returning to the prediction made in 1965, the author would like to formulate the following
hypothesis: there exists a connection between the mitochondrial DNA and the Y-chromosome that serves as
a gateway for (or a generator of) mutations induced and directed by the ecological differential rather than by
spontaneous mutations. This conclusion may be regarded as a program for future research.
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Severtsov Institute of Ecology and Evolution,
Russian Academy of Sciences,
Leninskii, 33, 117071 Moscow,
Russia